Impact, recovery and carryover effect of Roundup® on predator recognition in common spiny loach, Lepidocephalichthys thermalis

Abstract

Understanding the negative impact of a variety of environmental contaminants on aquatic animals is essential to curb biodiversity loss and stop degradation of ecological functions. Excessive and unrestricted use of pesticides is the most serious threat to aquatic animals including amphibians and fishes. Among the known pesticides, glyphosate based formulations have been shown to have lethal effects on many aquatic organisms. However, negative effects of pesticides on crucial ecological interactions such as prey-predator interactions are relatively unknown from tropics. In many aquatic organisms, recognition of predators is based on odor signatures; and therefore any anthropogenic alteration in water chemistry has the potential to impair recognition and learning of predators. Through a series of behavioral experiments we evaluated the effect of glyphosate based herbicide (Roundup®) on the antipredator behavior of common spiny loach, Lepidocephalichthys thermalis to understand the effects of pesticide-exposure on recognition of conspecific alarm cues, and associative learning to avoid predation. We exposed common spiny loach (for 3 h or 15 days) to sub-lethal concentration (0.5 mg a.e./L) of Roundup® and subsequently with conspecific alarm cues, signaling the proximity of a predator. Unexposed prey fish showed a significant reduction in activity level in response to conspecific alarm cues. Whereas such alarm response was not observed in prey fish that were exposed to Roundup® either for 3 h or 15 days. Such lack of response could be associated with alteration of olfactory function in prey individuals. However, this inability to detect the conspecific alarm cues was found to be transient and exposed fish recovered within 2 days. In subsequent experiments, we showed that Roundup® deactivates the conspecific alarm cues thus making them unavailable for prey to evoke the response. Furthermore, Roundup® mediated degradation of conspecific alarm cues and diminished the associative learning necessary for detection of the invasive/unknown/novel predators. Overall, due to the worldwide occurrence of glyphosate in water bodies, glyphosate mediated behavioral suppression exposes the prey animals to a considerable risk of predation, both by native and non-native predators.

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Acknowledgements

We thank anonymous reviewers and subject editor for constructive comments and highly valuable suggestions on the earlier version of the manuscript. The research was supported by grants from University Grant Commission (UGC) under minor research project, file number 47-914/14 (WRO) New Delhi and Department of Biotechnology (DBT), Government of India under DBT-STAR College scheme awarded to Modern College of Arts, Science and Commerce, Ganeshkhind, Pune. We also thank Aditya Manek, Jayshree Menon, Nikhil Gaitonde, and Anuradha Batabyal for their help to improve the language quality of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable national and institutional guidelines for the care of use of animals were followed.